Acta Anaesthesiol Scand 2013; 57: 1124–1130 Printed in Singapore. All rights reserved

© 2013 The Acta Anaesthesiologica Scandinavica Foundation. Published by John Wiley & Sons Ltd ACTA ANAESTHESIOLOGICA SCANDINAVICA

doi: 10.1111/aas.12167

Ultrasound measurement of subglottic diameter and an empirical formula for proper endotracheal tube fitting in children E. J. Kim, S. Y. Kim, W. O. Kim, H. Kim and H. K. Kil Department of Anaesthesiology and Pain Medicine, Anaesthesia and Pain Research Institute, Yonsei University College of Medicine, Seoul, Korea

Background: The appropriate endotracheal tube (ETT) size is commonly determined using age-based formula; ETT size determination based on ultrasound (US) measurement of subglottic diameter (SD), the narrowest portion of the paediatric upper airway, may provide a better method for accurate fit. We aimed to validate ETT size determination using US measures of SD before intubation to establish an empirical formula for ETT fitting based on SD and biographic parameters. Methods: We included 215 children aged 1–72 months undergoing general anaesthesia. US was performed on the anterior neck to measure SD during mask ventilation under anaesthesia. Endotracheal intubation was performed with a cuffed ETT selected by age-based recommendation; the transverse outer diameter (OD) of the ETT within the trachea at the subglottis level (OD-ETT at SD) was measured. Results: The OD-ETT at SD was correlated with the actual OD-ETT outside the trachea (R2 = 0.635), showing the validity of

ultrasonographic measurement; moreover, the US-measured SD revealed strong correlation with the actual OD-ETT (R2 = 0.834). US-measured SD and biographic data (age, height and weight) showed little correlation in children less than 12 months but good correlation (age, height) in children older than 12 months (P < 0.01). Conclusions: US-measured OD-ETT at SD was in good agreement with the actual OD-ETT, suggesting that US-measured SD helps in choosing the appropriate ETT diameter for children. In children older than 12 months, the equation ‘OD (mm) = 0.01 × age (months) + 0.02 × height (cm) + 3.3’ may help select the appropriate ETT.

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required ETTs is more adequate than using the ID, when considering that outer portion of the ETT is where it closely meets patient’s airway. Ultrasound (US) measurement of the subglottic diameter (SD) at the cricoid cartilage level, the narrowest portion of the upper airway in children, may be a better method for determining the appropriate ETT size.1–4 Three recent publications reported that US-measured SD can be used as a guide for the selection of ETT in children.4–6 The primary aim of this study is to test the validity of US measurement of the SD prior to tracheal intubation for determining the appropriate ETT. However, Husein et al. suggested that US underestimates the SD, and therefore is inferior to video-bronchoscopic measurement.7 Although US provides distance measurements that are accurate as ± 1.0 mm,8,9 a difference of 1–2 mm is crucial in selecting the proper ETT size for children.

etermination of appropriate-sized endotracheal tube (ETT) is essential for anaesthesia in children. A tube with overly large diameter may result in subglottic oedema, followed by respiratory difficulty, while an undersized ETT can cause inappropriate ventilation, underestimation of end-tidal CO2 or leakage of anaesthetic gas. The most commonly used method for determining the proper uncuffed ETT size, the modified Cole formula [size (mm, internal diameter, ID) = age/4 + 4] for uncuffed ETT, can be practical and easy to use.1–3 For cuffed ETT, Motoyama’s formula (ID = age/4 + 3.5) or the formula by Khine et al. (ID = age/4 + 3) can be recommended. But such formula can have its limitation in all-aged children probably due to the variety of airway development by growing. It provides the age-appropriate ID of ETT. However, we feel that estimating the outer diameter (OD) of the

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Accepted for publication 7 July 2013 © 2013 The Acta Anaesthesiologica Scandinavica Foundation. Published by John Wiley & Sons Ltd

Formula for endotracheal tube fitting

A

B

C Fig. 1. Ultrasound images of the airway: (A) Image at the hyoid bone level. The hyoid bone appears as an inverted U-shaped hyperechoic curvilinear line (arrowheads). (B) Image at the vocal cord level. (C) Image at the cricoid cartilage level. The cricoid cartilage appears as an arched, rounded hypoechoic structure (asterisks). SM, strap muscle; VL, vocal ligaments; AC, arytenoid cartilage; VM, vocalis muscle; TG, thyroid gland; CTA, comet tail artefacts.

Thus, it is necessary to verify the accuracy of US measurements in choosing the appropriate ETT by statistical correlation analysis. The second goal of this study is to generate an equation for predicting the appropriate ETT based on US-measured SD.

Materials and methods US evaluation of airway dimensions This study was approved by the internal review board of the Yonsei University Health System (IRB number: 4-2009-0723) and was registered at ClinicalTrials.gov (ref:NCT01227161)*. We recruited 227 children age 1–72 months scheduled for urological surgery with general endotracheal anaesthesia in this study. Written informed consent was obtained from the parents. Patients with a previous history of tracheostomy, airway obstruction or other airway anatomical abnormalities, and patients expected to be difficult to intubate for other reasons, were excluded. *http://www.clinicaltrials.gov

Anaesthesia was induced with 7–8% sevoflurane in 100% oxygen or by intravenous administration of 2–2.5 mg kg−1 propofol. Patients were laid in the supine position. The head was maintained in a neutral position with slight extension using 3 cm of rolled-cotton pad under the neck for every patient. After loss of consciousness, 0.4 mg kg−1 atracurium was administered for muscle relaxation. While the anaesthesiologist mask-ventilated the patient’s lungs, US was performed in B mode (brightness mode, two-dimensional image) with a linear probe (40 mm length; frequency range, 8–13 MHz; LOGIQeTM, GE Healthcare, Wauwatosa, WI, USA) placed on the midline of the anterior neck. The evaluation began by identifying the hyoid bone, which appeared as a superficial, hyperechoic curvilinear structure with posterior acoustic shadowing in the transverse view (Fig. 1A). Thereafter, the probe was moved caudally at a slight cephalad angle to locate the vocal muscles (two triangular hypoechoic structures) outlined medially by the hyperechoic vocal ligaments (Fig. 1B) and the archlike appearance of the cricoid cartilage with a bright

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air–mucosa interface (Fig. 1C). During US imaging, the anaesthesiologist stopped mask ventilation to acquire clear, still images; however, it was not stopped for more than 5 s to avoid possible hypoventilation. The same highly experienced anaesthesiologist performed all the US examinations in this patient series. After obtaining US images, each patient was intubated with a cuffed ETT (Hi-ContourTM, Mallinckrodt, Pleasanton, CA, USA) selected by an age-based recommendation (Table 1).10 ETT was inserted without any resistance in all children, and air leak test was not performed. Thereafter, US imaging was repeated, as described, to measure the OD-ETT within the trachea at the subglottic level just below the cricoid cartilage (OD-ETT at SD). The images were recorded three times at each tracheal level and stored for later analysis. An independent US specialist blind to both the goal of this study and each patient’s ETT size measured the relevant subglottic distances on the stored US images. The transverse diameter of the subglottis was measured between the bilateral margins of the

Statistical analysis Data analysis was performed using PASW Statistics 18 (SPSS Inc., Chicago, Il, USA). The primary end point of this study was to obtain the degree of agreement between the US-measured OD-ETT at SD and the actual (manufacturer’s) OD-ETT using the Bland–Altman method to verify the accuracy of US measurements. The secondary end point of this study was to derive an empirical relationship between the patient’s biographic parameters (age, weight and height) and the SD. Pearson’s coefficient and simple/multiple linear regression analyses were used to derive empirical relationships with statistical validity.

Results

Table 1 Manufacturers’ recommended endotracheal tube diameters for children10 and the OD-ETTs used in this study. OD varies among different manufacturers. Age

ID of ETT (mm)

OD of ETT (mm)

Premature (< 1250 g) Full term 1 year 2 years 6 years

2.5 uncuffed 3.0 uncuffed 3.5–4.0 cuffed 4.5–5.0 cuffed 5.0–5.5 cuffed

3.3 4.3 4.9–5.6 6.2–6.8 6.8–7.6

ID, internal diameter; ETT, endotracheal tube; OD, outer diameter.

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mid-cricoid cartilage beyond the air–mucosa interface (Fig. 2A). The transverse diameter was chosen, other than the anterior-posterior (AP) diameter due to the ambiguous image of the posterior portion of the airway with regard to the posterior acoustic shadowing by the adjacent tissues. Three measured values of transverse diameter were averaged for each patient. The transverse OD of the inserted ETT was defined as the maximum distance between the outer ETT walls (Fig. 2B).

Patient characteristics are presented in Table 2. US evaluation was well tolerated by every patient, and no adverse events occurred during intubation. Twelve patients were eliminated from the study: two, because no intubation was performed, and 10 due to missing data. The final dataset was derived from 215 intubated children. In 14 of the 215 patients (0.74%), the US-measured SD values were less than the actual OD-ETT, but none of these cases either exhibited resistance

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Fig. 2. Ultrasound images of the airway: (A) Image at the subglottic level before endotracheal intubation. The transverse diameter of the subglottis (dotted line) is between the transverse edges of the cricoid cartilage (asterisks). (B) Image at the subglottic level after endotracheal intubation. The transverse OD-ETT is the distance between the outer walls of the ETT (arrows). TG, thyroid gland; SM, strap muscle.

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Formula for endotracheal tube fitting Table 2 Patient characteristics. Number of patients Weight (kg) Height (cm)

0–6 months

6–12 months

1–2 years

2–3 years

> 3 Years

22 7.3 ± 2.1 64.8 ± 6.2

57 8.8 ± 1.1 71.3 ± 4.5

64 11.3 ± 2.2 80.8 ± 6.3

30 13.3 ± 2.3 89.8 ± 7.8

42 16.3 ± 3.3 100.9 ± 11.9

Data are mean ± standard deviation unless otherwise stated.

Fig. 3. Bland–Altman precision analysis of the differences between ultrasound-measured OD-ETT at SD and the actual OD-ETT. The limits of agreement are 0.71 mm and −1.03 mm. OD, outer diameter; US, ultrasound; ETT, endotracheal tube.

during the passage of the ETT past the cricoid level during intubation, or showed stridor or excessive cough during and after extubation. The US-measured OD-ETT at SD was in close agreement with the actual OD-ETT as revealed by Bland–Altman precision analyses (Fig. 3). Overall, 95.3% of the differences between the mean ODs of the two distances were distributed in a limit of agreement of 0.71 mm and −1.03 mm (mean difference ± 1.96 SD). The R2 value from simple linear regression was 0.635. Moreover, 96.3% of differences between the US-measured SD and US-measured OD-ETT at SD were within 1.49 mm and −0.48 mm (Fig. 4). Simple linear regression analysis revealed good correlations between the US-measured SD, and both the actual OD-ETT (R2 = 0.834) and the US-measured OD-ETT at SD (R2 = 0.425). Backward stepwise multiple regression analysis revealed little correlation between the US-measured SD and the biographic data (age, height and weight) for children younger than 12 months; however, the

Fig. 4. Bland–Altman precision analysis of the differences between ultrasound-measured SD and the ultrasound-measured OD-ETT at SD. The limits of agreement are 1.49 mm and −0.48 mm. SD, subglottic diameter; OD, outer diameter; ETT, endotracheal tube; US, ultrasound.

US-measured SD correlates with age and height in children older than 12 months.

Discussion The primary purpose of this study was to verify whether US-measured SD can be applied in selecting the ETT diameter in children. Although the error in distance measurement by US is less than ± 1.0 mm,8,9 this level may be insufficient for ETT selection as the OD of each ETT varies by 0.5 mm among the manufacturers. We evaluated the agreement between the US-measured OD-ETT within the trachea and the actual OD-ETT, and found that 95.3% of the differences between these values were within the limit of agreement of 0.71 mm and −1.03 mm (Fig. 3). Although the corrected R2 value was 0.635 of the two measurements, this limit of agreement shows the high reliability of US for measuring airway distances and suggests that US-measured SD can be helpful in choosing the appropriate OD-ETT.

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US is a useful device in airway evaluation, particularly in assessing the SD.4,5,11 The hyoid bone is the only completely ossified laryngeal structure in children,12 while thyroid cartilage, cricoid cartilage and the greater part of the arytenoid cartilage consist of hyaline cartilage that undergoes calcification and ossification with age.13 Although inadequate calcification of paediatric laryngeal structures may limit the spatial resolution of US, this does not alter the results. Furthermore, the advantages of US over other imaging modes, such as magnetic resonance imaging (MRI), computed tomography (CT) or radiographs, cannot be disregarded: less radiation, non-invasiveness, portability and accessibility.13 In this study, we measured the transverse diameter for subglottic distance. AP diameter cannot be accurately measured on US due to the posterior acoustic shadowing from the adjacent tissues.11,14 As the transverse diameter is slightly smaller than the AP diameter due to the oval shape of the subglottis,15,16 measuring the transverse diameter of the subglottis should be best for predicting the maximum allowable ETT diameter. Husein et al. reported that US always underestimates the SD in children.7 However, their result could be the consequence of measuring the transverse distance at ambiguous points on US. The cricoid cartilage appeared as a round hypoechoic structure (medulla) with hyperechoic edges (internal and external perichondrium) in the transverse view.5,11 For accurate measurement of SD, the transverse distance of the air column should be measured at the cricoid cartilage level after confirming the tracheal lumen, rather than the distance between the bilateral extreme edges of the hyperechoic shadow.11,17,18 Three previous studies assessed the usefulness of US for the selection of ETT in children.4–6 In a welldesigned study of Shibasaki et al., the US-measured SD and the OD-ETT showed a very strong correlation (R2 = 0.9). However, despite the higher R2 value, the limits of agreement were wider than the limits reported in our study (2 mm and −5.7 mm vs. 1.49 mm and −0.48 mm) (Fig. 4). As mentioned earlier, SD should be measured by recognizing the air–mucosa interface at the cricoid level.5,6,11,17 Shibasaki et al. did not present the measuring point in Fig. 2A of their study, in which a dotted line defined as ‘SD’ is marked at the bilateral margin of the cricoid cartilage beyond the air–mucosa interface.4 In fact, if SD was measured between the margins of the cricoid cartilage, a high correlation of the two distances should be expected. Bae et al. asserted that the reliability of US for determination

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of appropriate ETT is limited, even though the rate of correct tube was higher in US-selected cases compared with age-based selected cases (60% vs. 31%).5 However, their findings alone are not enough to ascertain the reliability of US. The second goal of our study was to generate an equation for predicting the appropriate ETT size. Paediatric anaesthesiologists often choose the ETT size either empirically or using the classical standard formulas (Cole’s, Motoyama’s or the formula by Khine et al.),1–3 but those formulas deal with the ID for selecting ETT. Most commercialized ETTs have their ID predetermined and the wall thickness varies by manufacturers. Such difference in wall thickness increases as the ID of ETT grows.19 Recently, Schramm et al. reported that US-measured SD was more predictable (48%) in uncuffed ETT selection than age-based formulas (40% and 24%),6 but the overall predictability was relatively low (48%) for several types of ETT they used. Therefore, we thought that applying the OD is more reliable to select ETT than using the ID, when considering that the outer portion of the ETT is where it closely meets patient’s airway. In this study, US-measured SD showed no significant correlation with demographic parameters in children younger than 12 months, while SD showed a significant correlation with age and height in children older than 12 months. We could get the equation of ‘SD (mm) = 0.01 × age (months) + 0.02 × height (cm) + 4.3’. For free passage of a cuffed ETT through the subglottis, it would be appropriate to select an ETT with diameter 1 mm smaller than the calculated SD, although it is recommended that the presence of a deflated cuff adds about 0.5 mm to the calculated OD of ETT.20 Thus, ‘OD (mm) = 0.01 × age (months) + 0.02 × height (cm) + 3.3’ may yield a reasonable estimate of appropriate ETT diameter for children older than 12 months. The paediatric airway is markedly changed during infancy, and becomes a characteristic adult airway by the age of 8. Thus, it may be difficult to predict the airway diameter in infants compared with older children. In other previously published 22 studies (including von Rettberg group), the similar results were reported.21 US image can be affected with a pressure applied on the skin by the probe and the thickness of the fat on the anterior neck in children.22 Neck position does influence subglottic dimensions as well. For these aspects, if the discrepancy in the measurements was significant, the agreement between the US-measured OD-ETT at SD and the actual OD-ETT could not be attained.

Formula for endotracheal tube fitting

In this study, tracheal intubation was performed with a cuffed tube in all cases to avoid the possibility of ETT misplacement during the positional change for caudal or epidural block used for post-operative analgesia. While many studies have conducted air leak test to evaluate the ‘best fit’ ETT size, we have omitted such process for the main objects of this study being the pursuit of accurate US measurement and the derivation of equation using measured value. We have selected the ETT size according to an age-based recommendation by the textbook (Table 1), and each intubation process was done without any resistance. In this study, the strong correlation between the US-measured SD and OD-ETT at SD supports the usefulness of US in proper ETT size determination. But such measurements only reflect the twodimensional distance, and the question whether ETTs are properly fitted needs to be further discussed or be referred to other test methods, such as air leak test. Although few studies suggested that the airway diameter at the glottis level is narrower at the subglottic level,15,16 recent studies using MRI and CT demonstrated that the subglottis is the narrowest portion of the airway in young (< 2 years) children.12,23 In addition, the trachea at the subglottic level exhibits limited distension due to the surrounding cricoids cartilage. It is essential that ETT size should not be greater than the SD. Despite the many virtues of US, there is another weakness: the operator dependency. We believe such method can be used in clinical setting, once the reproducibility and learning curve for US are achieved by the operator. Due to the limitation of practicality and familiarity of US, our method could be less accessible in everyday clinical practice. In contrast, its strength on precise measurement can be taken into account when determining the proper ETT size for neonates, infants or children with known anatomical distortion or previous history of difficult intubation. In using US for neonate and infants, the equation ‘ETT OD (mm) = 0.55 × SD on ultrasound (mm) + 1.16’ suggested by Shibasaki et al. can be helpful.4 In conclusion, the US-measured SD can be useful for choosing the appropriate size of ETT for children. If US is not available in the clinical setting, the equation ‘OD (mm) = 0.01 × age (months) + 0.02 × height (cm) + 3.3’ may be helpful for selecting the proper ETT for children older than 12 months of age. Conflict of interest: The authors have no conflicts of interest.

Funding: This study was partly supported by a grant from the Korea Healthcare Technology R&D Project, Ministry for Health, Welfare & Family Affairs, Republic of Korea (A084120).

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23. Al Mazrou KA, Abdullah KM, Ansari RA, Abdelmeguid ME, Turkistani A. Comparison of the outer diameter of the ‘best-fit’ endotracheal tube with MRI-measured airway diameter at the cricoid level. Eur J Anaesthesiol 2009; 26: 736–9.

Address: Professor Hae Keum Kil Department of Anaesthesiology and Pain Medicine Anaesthesia and Pain Research Institute Yonsei University College of Medicine 50 Yonsei-ro Seodaemun-gu Seoul 120-752 Korea e-mail: [email protected]

Ultrasound measurement of subglottic diameter and an empirical formula for proper endotracheal tube fitting in children.

The appropriate endotracheal tube (ETT) size is commonly determined using age-based formula; ETT size determination based on ultrasound (US) measureme...
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